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Prenatal hypoxia increases blood pressure in male rat offspring and affects their response to artificial light at night

Published online by Cambridge University Press:  28 October 2020

Hana Sutovska ,
Lubos Molcan Open the ORCID record for Lubos Molcan [Opens in a new window] ,
Romana Koprdova ,
Michaela Piesova ,
Mojmír Mach  and
Michal Zeman
Hana Sutovska
Affiliation:
Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia
Lubos Molcan*
Affiliation:
Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia
Romana Koprdova
Affiliation:
Centre of Experimental Medicine SAS, Institute of Experimental Pharmacology and Toxicology, Slovak Academy of Sciences, Bratislava, Slovakia
Michaela Piesova
Affiliation:
Centre of Experimental Medicine SAS, Institute of Experimental Pharmacology and Toxicology, Slovak Academy of Sciences, Bratislava, Slovakia Department of Pharmacology, Jessenius Faculty of Medicine, Comenius University, Martin, Slovakia
Mojmír Mach
Affiliation:
Centre of Experimental Medicine SAS, Institute of Experimental Pharmacology and Toxicology, Slovak Academy of Sciences, Bratislava, Slovakia
Michal Zeman
Affiliation:
Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia
*
Address for correspondence: Lubos Molcan, Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University in Bratislava, Ilkovicova 6, Bratislava, Slovakia. Email: lubos.molcan@uniba.sk
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Abstract

Prenatal hypoxia (PH) has negative consequences on the cardiovascular system in adulthood and can affect the responses to additional insults later in life. We explored the effects of PH imposed during embryonic day 20 (10.5% O2 for 12 h) on circadian rhythms of systolic blood pressure (BP) and heart rate (HR) in mature male rat offspring measured by telemetry. We evaluated: (1) stability of BP and HR changes after PH; (2) circadian variability of BP and HR after 2 and 5 weeks of exposure to artificial light at night (ALAN; 1–2 lx); and (3) response of BP and HR to norepinephrine. PH increased BP in the dark (134 ± 2 mmHg vs. control 127 ± 2 mmHg; p = 0.05) and marginally in the light (125 ± 1 mmHg vs. control 120 ± 2 mmHg) phase of the day but not HR. The effect of PH was highly repeatable between 21- and 27-week-old PH male offspring. Two weeks of ALAN decreased the circadian variability of HR (p < 0.05) and BP more in control than PH rats. After 5 weeks of ALAN, the circadian variability of HR and BP were damped compared to LD and did not differ between control and PH rats (p < 0.05). Responses of BP and HR to norepinephrine did not differ between control and PH rats. Hypoxia at the end of the embryonic period increases BP and affects the functioning of the cardiovascular system in mature male offspring. ALAN in adulthood decreased the circadian variability of cardiovascular parameters, more in control than PH rats.

Keywords

Blood pressureheart rateprenatal hypoxiaartificial light at night
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 4 , August 2021 , pp. 587 - 594
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Copyright
© The Author(s), 2020. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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References

Giussani, DA, Davidge, ST. Developmental programming of cardiovascular disease by prenatal hypoxia. J Dev Orig Health Dis. 2013; 4, 328–337.CrossRefGoogle ScholarPubMed
Kumar, P, Morton, JS, Shah, A, et al. Intrauterine exposure to chronic hypoxia in the rat leads to progressive diastolic function and increased aortic stiffness from early postnatal developmental stages. Physiol Rep. 2020; 8, e14327.CrossRefGoogle ScholarPubMed
Andraweera, PH, Gatford, KL, Care, AS, et al. Mechanisms linking exposure to preeclampsia in utero and the risk for cardiovascular disease. J Dev Orig Health Dis. 2020; 1–8.CrossRefGoogle ScholarPubMed
Giussani, DA, Camm, EJ, Niu, Y, et al. Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS ONE. 2012; 7, e31017.CrossRefGoogle ScholarPubMed
Verschuren, MTC, Morton, JS, Abdalvand, A, et al. The effect of hypoxia-induced intrauterine growth restriction on renal artery function. J Dev Orig Health Dis. 2012; 3, 333–341.CrossRefGoogle ScholarPubMed
Alma, LJ, De Groot, CJM, De Menezes, RX, et al. Endothelial dysfunction as a long-term effect of late onset hypertensive pregnancy disorders: high BMI is key. Eur J Obstet Gynecol Reprod Biol. 2018; 225, 62–69.CrossRefGoogle ScholarPubMed
Tain, Y-L, Huang, L-T, Hsu, C-N. Developmental programming of adult disease: reprogramming by melatonin? Int J Mol Sci. 2017; 18, 426.CrossRefGoogle ScholarPubMed
Svitok, P, Molcan, L, Stebelova, K, et al. Prenatal hypoxia in rats increased blood pressure and sympathetic drive of the adult offspring. Hypertens Res. 2016; 39, 501–505.CrossRefGoogle ScholarPubMed
Van den Bergh, BR, van den Heuvel, MI, Lahti, M, et al. Prenatal developmental origins of behavior and mental health: the influence of maternal stress in pregnancy. Neurosci Biobehav Rev. Epub ahead of print 28 July 2017. doi: 10.1016/j.neubiorev.2017.07.003.Google Scholar
Shah, A, Matsumura, N, Quon, A, et al. Cardiovascular susceptibility to in vivo ischemic myocardial injury in male and female rat offspring exposed to prenatal hypoxia. Clin Sci. 2017; 131, 2303–2317.CrossRefGoogle ScholarPubMed
Zeman, M, Okuliarova, M. Sex-specific cardiovascular susceptibility to ischaemic myocardial injury following exposure to prenatal hypoxia. Clin Sci. 2017; 131, 2791–2794.CrossRefGoogle ScholarPubMed
Smolensky, MH, Hermida, RC, Portaluppi, F. Circadian mechanisms of 24-hour blood pressure regulation and patterning. Sleep Med Rev. 2017; 33, 4–16.CrossRefGoogle ScholarPubMed
Black, N, D’Souza, A, Wang, Y, et al. Circadian rhythm of cardiac electrophysiology, arrhythmogenesis, and the underlying mechanisms. Heart Rhythm. 2019; 16, 298–307.CrossRefGoogle ScholarPubMed
Coomans, CP, Ramkisoensing, A, Meijer, JH. The suprachiasmatic nuclei as a seasonal clock. Front Neuroendocrinol. 2015; 37, 29–42.CrossRefGoogle ScholarPubMed
Molcan, L, Vesela, A, Zeman, M. Repeated phase shifts in the lighting regimen change the blood pressure response to norepinephrine stimulation in rats. Physiol Res. 2014; 63, 567–575.CrossRefGoogle ScholarPubMed
Chellappa, SL, Vujovic, N, Williams, JS, Scheer, FA. Impact of circadian disruption on cardiovascular function and disease.Trends Endocrinol Metab. 2019; 30, 767–779.CrossRefGoogle ScholarPubMed
Obayashi, K, Saeki, K, Iwamoto, J, Ikada, Y, Kurumatani, N. Association between light exposure at night and nighttime blood pressure in the elderly independent of nocturnal urinary melatonin excretion. Chronobiol Int. 2014; 31, 779–786.CrossRefGoogle ScholarPubMed
Molcan, L, Sutovska, H, Okuliarova, M, et al. Dim light at night attenuates circadian rhythms in the cardiovascular system and suppresses melatonin in rats. Life Sci. 2019; 231, 116568.CrossRefGoogle ScholarPubMed
Rumanova, VS, Okuliarova, M, Molcan, L, Sutovska, H, Zeman, M. Consequences of low-intensity light at night on cardiovascular and metabolic parameters in spontaneously hypertensive rats. Can J Physiol Pharmacol. 2019; 97, 863–871.CrossRefGoogle ScholarPubMed
Ujhazy, E, Dubovicky, M, Navarova, J, et al. Subchronic perinatal asphyxia in rats: embryo–foetal assessment of a new model of oxidative stress during critical period of development. Food Chem Toxicol. 2013; 61, 233–239.CrossRefGoogle ScholarPubMed
Zuther, P, Gorbey, S, Lemmer, B. Chronos-Fit 1.06. Chronos-Fit. 2009. http://www.ma.uni-heidelberg.de/inst/phar/lehre/chrono.html.Google Scholar
Schulz, LC. The Dutch Hunger Winter and the developmental origins of health and disease. Proc Natl Acad Sci. 2010; 107, 16757–16758.CrossRefGoogle Scholar
Eckhart, AD, Zhu, Z, Arendshorst, WJ, Faber, JE. Oxygen modulates alpha 1B-adrenergic receptor gene expression by arterial but not venous vascular smooth muscle. Am J Physiol-Heart Circ Physiol. 1996; 271, H1599–H1608.CrossRefGoogle Scholar
Hutchinson, DS, Brew, N, Vu, T, et al. Effects of hypoxia-ischemia and inotropes on expression of cardiac adrenoceptors in the preterm fetal sheep. J Appl Physiol. 2018; 125, 1368–1377.CrossRefGoogle ScholarPubMed
Moretta, D, Papamatheakis, DG, Morris, D, et al. Long-term high altitude hypoxia and alpha adrenoceptor-dependent pulmonary arterial contractions in fetal and adult sheep. Front Physiol. 2019; 10, 1032.CrossRefGoogle ScholarPubMed
Chen, X, Zhang, L, Wang, C. Prenatal hypoxia-induced epigenomic and transcriptomic reprogramming in rat fetal and adult offspring hearts. Sci Data. 2019; 6, 1–8.CrossRefGoogle ScholarPubMed
Chen, X, Qi, L, Fan, X, et al. Prenatal hypoxia affected endothelium-dependent vasodilation in mesenteric arteries of aged offspring via increased oxidative stress. Hypertens Res. 2019; 42, 863–875.CrossRefGoogle ScholarPubMed
Walton, SL, Bielefeldt-Ohmann, H, Singh, RR, et al. Prenatal hypoxia leads to hypertension, renal renin-angiotensin system activation and exacerbates salt-induced pathology in a sex-specific manner. Sci Rep. 2017; 7, 1–13.CrossRefGoogle Scholar
Svitok, P, Husková, Z, Červenková, L, et al. The exaggerated salt-sensitive response in hypertensive transgenic rats (TGR mRen-2) fostered by a normotensive female. Hypertens Res. 2019; 42, 459–468.CrossRefGoogle ScholarPubMed
Yang, K, Wang, Y, Ding, Y, et al. Valsartan chronotherapy reverts the non-dipper pattern and improves blood pressure control through mediation of circadian rhythms of the renin-angiotensin system in spontaneous hypertension rats. Chronobiol Int. 2019; 36, 1058–1071.CrossRefGoogle ScholarPubMed
Thosar, SS, Butler, MP, Shea, SA. Role of the circadian system in cardiovascular disease. J Clin Invest. 2018; 128, 2157–2167.CrossRefGoogle ScholarPubMed
Nishi, EE, Almeida, VR, Amaral, FG, et al. Melatonin attenuates renal sympathetic overactivity and reactive oxygen species in the brain in neurogenic hypertension. Hypertens Res Off J Jpn Soc Hypertens. 2019; 42, 1683–1691.CrossRefGoogle ScholarPubMed
Coote, JH. A role for the paraventricular nucleus of the hypothalamus in the autonomic control of heart and kidney. Exp Physiol. 2005; 90, 169–173.CrossRefGoogle ScholarPubMed
Pyner, S, Coote, JH. Identification of branching paraventricular neurons of the hypothalamus that project to the rostroventrolateral medulla and spinal cord. Neuroscience. 2000; 100, 549–556.CrossRefGoogle ScholarPubMed
Fan, J-M, Wang, X, Hao, K, et al. Upregulation of PVN CRHR1 by gestational intermittent hypoxia selectively triggers a male-specific anxiogenic effect in rat offspring. Horm Behav. 2013; 63, 25–31.CrossRefGoogle ScholarPubMed
Raff, H, Jacobson, L, Cullinan, WE. Augmented hypothalamic corticotrophin-releasing hormone mRNA and corticosterone responses to stress in adult rats exposed to perinatal hypoxia. J Neuroendocrinol. 2007; 19, 907–912.CrossRefGoogle ScholarPubMed
Lindgren, I, Altimiras, J. Chronic prenatal hypoxia sensitizes β-adrenoceptors in the embryonic heart but causes postnatal desensitization. Am J Physiol-Regul Integr Comp Physiol. 2009; 297, R258–R264.CrossRefGoogle ScholarPubMed
Kostrzewa, RM. The blood-brain barrier for catecholamines — Revisited. Neurotox Res. 2007; 11, 261–271.CrossRefGoogle ScholarPubMed